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. 2023 Jan 25;30(15):44566–44577. doi: 10.1007/s11356-023-25383-0

Biosynthesized silver nanoparticles have anticoccidial and jejunum-protective effects in mice infected with Eimeria papillata

Mohamed A Dkhil 1,2, Felwa A Thagfan 3,✉, Mostafa Y Morad 1, Esam M Al-Shaebi 4, Sherif Elshanat 5, Amira A Bauomy 6, Murad Mubaraki 7, Taghreed A Hafiz 7, Saleh Al-Quraishy 4, Rewaida Abdel-Gaber 4
PMCID: PMC9873539  PMID: 36694067

Abstract

Eimeriosis, an infection with Eimeria spp. that affects poultry, causes huge economic losses. Silver nanoparticles (AgNPs) have antibacterial and antifungal properties, but their action against Eimeria infection has not yet been elucidated. This study demonstrates the action of AgNPs in the treatment of mice infected with Eimeria papillata. AgNPs were prepared from Zingiber officinale rhizomes. Phytochemical screening by gas chromatography–mass spectrometry analysis (GC–MS) was used to detect active compounds. Mice were divided into five groups: uninfected mice, uninfected mice that were administered AgNPs, untreated mice infected with 103 sporulated oocysts of E. papillata, infected mice treated with AgNPs, and infected mice treated with amprolium. Characterization of the samples showed the AgNPs to have nanoscale sizes and aspherical shape. Phytochemical screening by GC–MS demonstrated the presence of 38 phytochemical compounds in the extract of Z. officinale. Mice infected with E. papillata-sporulated oocysts were observed to have many histopathological damages in the jejuna, including a decrease in the goblet cell numbers affecting the jejunal mucosa. Additionally, an increased oocyst output was also observed. The treatment of infected mice with AgNPs resulted in the improvement of the jejunal mucosa, increase in the number of goblet cell, and decrease in the number of meronts, gamonts, and developing oocysts in the jejuna. Moreover, AgNPs also led to decreased oocyst shedding in feces. The results revealed AgNPs to have an anticoccidial effect in the jejunum of E. papillata-infected mice and, thus, could be a potential treatment for eimeriosis.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11356-023-25383-0.

Keywords: Coccidiosis, AgNPs, Zingiber officinale, Jejuna, Goblet cells, Mice

Introduction

Eimeria spp. are among the most destructive protozoans of the phylum Apicomplexa. Eimeria infection via fecal–oral transmission has mainly been associated with the disease coccidiosis. Interestingly, in cases of Eimeria infections, every part of the intestine has been observed to be infected with a specific Eimeria species (Lillehoj et al. 2015). The invasion of Eimeria sporozoites into the epithelial cells of the intestine of poultry animals results in diarrhea, malabsorption of nutrients leading to weight loss, and finally, death, thereby causing huge economic loss to the poultry industry (Alnassan et al. 2014). Eimeria papillata invades the jejunum of the mouse intestine (site of infection), leading to serious inflammation of the intestinal mucosa and increased oxidative conditions (Abdel-Latif et al. 2016). Therefore, this species is suitable for the evaluation of the impact of Eimeria infection in animal models (Dkhil 2013).

Nanotechnology is a promising research field having a variety of applications, especially in medicine and industry, (Zhao et al. 2017) with one of its most important applications being the control of a multitude of infectious diseases affecting animals and plants (Pimentel-Acosta et al. 2019; Resham et al. 2015). Silver nanoparticles (AgNPs) are considered to be efficient bactericidal, antifungal, and antiviral agents (Cho et al. 2018). In addition, AgNPs have good antiparasitic action against some protozoans infecting fishes like Ichthyophthirius multifiliis (Saleh et al. 2017). AgNPs can be synthesized by various chemical and physical methods that are known to be expensive, complex, and even involve toxic agents (Pimentel-Acosta et al. 2019). To overcome these issues, various techniques for the biosynthesis of AgNPs involving the use of different plants have been established as simple, eco-friendly, reliable, and inexpensive alternatives to chemical or physical methods (Bhakya et al. 2016).

The use of plant extracts enables NPs to be biosynthesized using specific plant parts instead of the whole plant. Extracts of various plants, such as aloe vera, ginger, honey, mango, amla, marigold, and lemon, have been reportedly used in the production and stabilization of NPs (Mehata 2021) Zingiber officinale rhizomes are widely used as a spice and for flavor in foods. They also have applications in the production of soaps, cosmetics, and more recently in medicine, such as in the treatment of coronavirus disease, stomach pain, cough, and in reducing the effect of acute chemotherapy-induced nausea in adult cancer patients (Ho et al. 2013; Semwal et al. 2015).

The present study aimed to evaluate the protective effect of AgNPs biosynthesized from Z. officinale on the jejunum in the intestines of mice infected with sporulated oocysts of Eimeria papillata.

Material and methods

Animals and parasite infection

Male mice (C57BL/6), aged 10–12 weeks, were used in this study. E. papillata oocysts were obtained from the feces of infected mice and were processed according to a method described in a previous study (Dkhil et al. 2011).

Preparation and phytochemical screening of Zingiber officinale extract

Z. officinale rhizomes were purchased from a market in Egypt. The plant specimens were validated by a taxonomist at the Department of Botany, Helwan University. The rhizomes were homogenized and subsequently used in the preparation of 70% Z. officinale methanolic extract (ZE) according to a method described by Thagfan et al. (2021).

The methanolic extract of ZE was subjected to gas chromatography–mass spectrometry analysis (GC–MS) using a Thermo Scientific™ Trace GC Ultra and ISQ™ Single Quadruple MS (Thermo Fisher Scientific, Waltham, USA) (Abdeen et al. 2019). Identification of the mass spectrum was conducted with reference to the Wiley Registry and National Institute Standard and Technology (NIST) databases.

Biosynthesis and characterization of silver nanoparticles

Briefly, AgNPs were biosynthesized by adding 45 mL of AgNO3 (8 × 10–3 M, ~ 0.06793 g) solution to approximately 5 mL of freshly prepared ZE and placing the mixture in a black chamber. The formation of AgNPs in the solution was ensured by incubating it until the color changed from brownish to black.

The absorbance of AgNPs was monitored by measuring the ultraviolet (UV)-visible spectra at wavelengths ranging from 300 to 800 nm with a UV-1650 PC UV–visible spectrophotometer (Shimadzu, Osaka, Japan). The form and size of AgNPs were characterized by transmission electron microscopy (TEM) using a JEOL JEM-2100 (JEOL Ltd., Tokyo, Japan) according to a method described by Jiang et al. (2008). The AgNP structure was characterized by X-ray diffraction (XRD) analysis (XRD-6000; Shimadzu). The XRD patterns were recorded at a scan speed of 4°/min.

In vivo infection and experimental design

Each mouse was infected with 103 sporulated E. papillata oocysts by oral administration, and the number of oocysts per gram of feces was calculated. Thirty-two mice were divided into five groups of eight mice each. The first group, representing the negative control group, was administered distilled water. The second group was administrated 5 mg/kg AgNPs daily via oral gavage inoculations (Abd El Wahab et al. 2021). The third, fourth, and fifth groups were infected with 103 E. papillata oocysts inoculated via oral route (Dkhil et al. 2015). After one hour of infection, the fourth and fifth groups were treated with orally administered AgNPs and 25 mg/kg amprolium, respectively, for 5 days.

On day 5, oocyst shedding was quantified using a McMaster chamber and was expressed as the number of oocysts per gram of wet feces. Subsequently, all mice were euthanized, and portions of the jejunum were preserved in formalin to count the parasite stages and goblet cells.

Enumeration of parasites

To count the parasite stages, all mice were sacrificed, and the jejunum portions were preserved in formalin. The jejunum specimens were embedded in paraffin wax and fixed in 10% buffered formalin. Subsequently, 4-μm-thick sections prepared using a microtome were stained with hematoxylin and eosin (HE). Oocysts per ten microvilli were then counted by observation under a light microscope.

Histopathology and enumeration of goblet cells

The jejunum was removed, processed, fixed in neutral buffered formalin for 12 h, dehydrated, and embedded in paraffin. The sections were stained with HE. Histological injury score was assessed according to a method described by Dommels et al. (2007).

The sections were stained with Alcian blue to estimate the number of goblet cells. The average number of goblet cells in 20 villi was calculated for each animal.

Statistical analysis

The data were analyzed using a one-way ANOVA, and statistical comparisons between groups were performed using Duncan’s test. Values are expressed as mean ± standard deviation (SD) at a significance level of P ≤ 0.05.

Results

Results of GC–MS at different retention times are presented in Table 1 and Figure S1 showing the detection of 38 active phytochemical compounds. The major compounds identified in ZE were 1-(4-hydroxy-3-methoxyphenyl)tetradec-4-en3-one (4.1%), (3R,5S)-1-(4-hydroxy-3-methoxyphenyl)decane-3,5-diyl diacetate (4.6%), 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6-methyl- (5.9%), butan-2-one, 4-(3-hydroxy-2-methoxyphenyl)- (17.4%), 1-(4-hydroxy-3-methoxyphenyl)dec-4-en-3-one (18.4%), and butan-2-one, 4-(3-hydroxy-2-methoxyphenyl)- (29.3%).

Table 1.

Effect of biosynthesized AgNPs on E. papilata developmental stages

Group Number of meronts Number of gamonts (males and females) Number of oocysts inside the epithelium
Infected 158.3 ± 35 26.5 ± 1 7.4 ± 3
Infected + ZNPs 57.2 ± 10* 15.6 ± 2.8* 1.2 ± 0.8*
Infected + Amp 79.8 ± 9* 17.4 ± 5* 2.6 ± 1.1*
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Data are mean ± SD in 10 villi. *,Significance against the infected group at p ≤ 0.05

TEM analysis showed that the size of the biosynthesized AgNPs was < 50 nm (Fig. 1). The formation of AgNPs was confirmed by observing color change from yellow to dark brown on addition of ginger extract to the AgNO3 solution. UV–visible spectroscopy for monitoring the production of AgNPs in the mixture revealed a strong and broad surface plasmon resonance peak at 450 nm, a characteristic feature of AgNPs (Fig. 2).

Fig. 1.

Fig. 1

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TEM of AgNPs showing their size. Scale bar = 100 nm

Fig. 2.

Fig. 2

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UV–Visible absorption spectrum of the biosynthesized AgNPs

Figure 3 shows the XRD patterns of AgNPs. All particles had similar diffraction profiles and XRD at different peaks.

Fig. 3.

Fig. 3

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X-ray diffraction pattern of biosynthesized AgNPs

After five days, mice infected with sporulated E. papillata oocysts had an oocyst output of approximately 70 × 104 oocysts/g of feces. AgNP treatment of infected mice led to a significant decrease in the oocyst output compared to that of the untreated infected group and the amprolium-treated group (Fig. 4).

Fig. 4.

Fig. 4

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Produced number of oocysts on day 5 postinfection. The values are represented as mean ± SD. *Significance against infected group at P < 0.05, n = 8

Histopathological changes were visible in the infected jejuna, particularly in the vacuolated injured jejunal mucosa, which contained lymphatic infiltration. In addition to observing the obvious destruction and shedding of jejunum epithelia caused by parasite invasion, the inflammatory status of the jejunum was assessed using a semi-quantitative scoring system. While the infected mice were reported to have mild inflammatory injury, AgNPs dramatically ameliorated the inflammatory lesions generated by E. papillata infection in mice (Fig. 5, Figure S2).

Fig. 5.

Fig. 5

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Histological changes during infection and after treatment with AgNPs. (A) Non-infected jejunum. (B) AgNP-treated jejunum. (C, D) Infected jejunum. Arrow head for parasitic stages of E. papillata. (E) Infected-treated jejunum treated with AgNPs. (F) Infected-treated Jejunum treated with Amp. Sections stained with H&E. Scale bar = 100 μm for A, B, C, E, and F. For D, the scale bar = 25 μm. N = 5

Analysis of the histological injury score showed inflammation in the jejunum of mice infected with E. papillata, and this inflammatory profile was significantly decreased after treatment with either AgNPs or amprolium (Fig. 6). Histological examinations of E. papillata-infected mice on day 5 post-infection showed a reduction in the number of goblet cells in comparison with that in the non-infected mice (Fig. 7). Treatment of infected mice with AgNPs significantly increased the number of goblet cells in the jejunal villi (Fig. 8).

Fig. 6.

Fig. 6

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The score of histological injury of the noninfected and Eimeria papillata-infected and Eimeria papillata-treated groups. The values are represented as mean ± SD. Significance against non-infected (*) and infected (#) group at P < 0.05

Fig. 7.

Fig. 7

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Goblet cells in the jejunum stained with Alcian blue, (A) control group, (B) AgNPs, and (C) infected group, while (D) and (E) are the treated groups with AgNPs and Amp, respectively. N = 5. Scale bar = 50 μm

Fig. 8.

Fig. 8

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The effect of treated mice with AgNPs or Amp on the number of jejunal goblet cells. N = 5. The values are represented as mean ± SD. Significance against non-infected (*) and infected (#) group at P < 0.05

The groups treated with AgNPs showed a significant decrease in the total number of parasitic stages in E. papillata-infected mice in comparison with that in the control group (Fig. 9). In addition, meronts, gamonts, and developed oocysts in the jejunum were significantly altered after treatment with AgNPs (Table 2).

Fig. 9.

Fig. 9

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Effect of treatment of E. papillata-infected mice with AgNPs and Amp. on the parasitic stages counting in 10 VCU/mouse. The values are represented as mean ± SD. Significance against non-infected (*) and infected (#) group at P < 0.05

Table 2.

Identification of phytochemical compounds by GC-Mass in Zingiber officinale extract

Component RT Compound name Molecular weight [M-H]- (m/z)
molecular weight-1		 Formula Area Peak %
1.1303 Dimethylamine 45.0837 44.0837 C2H7N 228,135,067 1.047661706
1.6259 Carbonic acid, ethyl 2-propenyl ester 130.1418 129.1418 C6H10O3 11,332,076 0.052040145
2.3007 Hexanal 100.1589 99.1589 C6H12O 126,339,131 0.580185551
2.5612 Acetic acid 60.0520 59.052 C2H4O2 313,764,424 1.440896291
3.3843 Cyclooctyl alcohol 128.2120 127.212 C8H16O 231,692,987 1.064000696
3.8265 3-Benzoyl-5-[2-(phenylthio)ethyl]-3,4- diazatricyclo[5.2.1.0(2,6)]dec-4-ene 376.5 375.5 C23H24N2OS 141,037,231 0.647683445
4.1020 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6- methyl- 144.1253 143.1253 C6H8O4 1,288,212,662 5.915842284
4.7163 Iso-Amyl tiglate 170.2487 169.2487 C10H18O2 473,929,136 2.176418619
5.0353 Eugenol 164.2011 163.2011 C10H12O2 144,068,476 0.661603792
5.9356 2,4-Di-tert-butylphenol 206.3239 205.3239 C14H22O 258,344,144 1.186390459
6.3324 (1S,2E,6E,10R)-3,7,11,11- Tetramethylbicyclo[8.1.0]undeca-2,6-diene 204.3511 203.3511 C15H24 162,634,245 0.746863132
6.7993 Pipecolic acid, N-ethoxycarbonyl-, octyl ester 313.4 312.4 C17H31NO4 551,771,665 2.533893854
7.1129 Butan-2-one, 4-(3-hydroxy-2-methoxyphenyl)- 194.2271 193.2271 C11H14O3 3,793,915,802 17.42275028
7.4459 4-(2,4-Dimethoxyphenyl)butan-2-one 208.254 207.254 C12H16O3 265,489,450 1.219203755
7.9909 Phenol, 5-(1,5-dimethyl-4-hexenyl)-2-methyl-, (R)- 218.3346 217.3346 C15H22O 43,033,343 0.197621462
8.3357 Benzene, 1-(1,1-dimethylethyl)-3,5-dimethyl- 162.2713 161.2713 C12H18 10,947,730 0.050275118
8.6704 3-Buten-2-one, 4-(4-hydroxy-3- methoxyphenyl)- 192.2112 191.2112 C11H12O3 149,937,296 0.688555098
9.0728 Hexanedioic acid, mono(2-ethylhexyl)ester 258.35 257.35 C14H26O4 156,441,793 0.718425615
9.6852 Hexadecanoic acid, methyl ester 270.4507 269.4507 C17H34O2 26,553,501 0.121941298
10.0130 n-Hexadecanoic acid 256.4241 255.4241 C16H32O2 52,125,672 0.239376047
10.5018 4-Morpholineacetonitrile,.alpha.-phenethylidene- 228.290 227.29 C14H16N2O 17,881,140 0.082115327
10.8850 (E)-1-(6,10-Dimethylundec-5-en-2-yl)-4-methylbenzene 272.47 271.47 C20H32 25,346,936 0.116400405
11.4534 1-(4-Hydroxy-3-methoxyphenyl)oct-4-en-3-one 248.3175 247.3175 C15H20O3 37,056,022 0.170171889
12.4495 2-Butanone, 4-(4-hydroxy-3-methoxyphenyl)- 194.2271 193.2271 C11H14O3 134,101,729 0.615833629
12.9815 3-Decanone, 1-(4-hydroxy-3-methoxyphenyl)- 278.3865 277.3865 C17H26O3 337,285,165 1.548910284
13.5979 1-(4-Hydroxy-3-methoxyphenyl)dec-4-en-3-one 276.3707 275.3707 C17H24O3 4,020,860,357 18.46494482
13.9098 1-(4-Hydroxy-3-methoxyphenyl)decane-3,5- dione 292.4 291.4 C17H24O4 106,745,446 0.490205726
14.2833 Butan-2-one, 4-(3-hydroxy-2-methoxyphenyl)- 194.2271 193.2271 C11H14O3 6,399,413,510 29.38794358
14.9799 (3R,5S)-1-(4-Hydroxy-3-methoxyphenyl)decane-3,5-diyl diacetate 380.4752 379.4752 C21H32O6 1,021,953,670 4.693104571
15.4564 5-Hydroxy-1-(4-hydroxy-3-methoxyphenyl)dodecan-3-one 322.4 321.4 C19H30O4 178,446,849 0.819479148
16.1382 1-(4-Hydroxy-3-methoxyphenyl)tetradec-4-en3-one 332.5 331.5 C21H32O3 894,238,903 4.106601705
16.4355 1-(4-Hydroxy-3-methoxyphenyl)tetradecane-3,5-dione 348.5 347.5 C21H32O4 97,502,585 0.447759855
16.9058 2-Butanone, 4-(4-hydroxy-3-methoxyphenyl)- 194.2271 193.2271 C11H14O3 13,262,060 0.060903186
17.4487 4(1H)-Quinolone, 2,3-dihydro-6-methoxy-2- methyl-1-(p-tolylsulfonyl)- 345.4 344.4 C18H19NO4S 6,243,408 0.028671522
17.8666 Caprolactone oxime, (NB)-O- [(diethylboryloxy)(ethyl)boryl]- C12H25B2NO2 37,389,839 0.171704872
18.5173 Alanine, N-methyl-N-(2-chloroethoxycarbonyl)-, pentadecyl ester 420.0 419 C22H42ClNO4 16,385,364 0.075246294
19.1360 2-Hydroxy-6-methyl-2-trifluoromethyl-4Hbenzo[1,4]oxazin-3-one 247.17 246.17 C10H8F3NO3 1,467,144 0.006737546
19.7918 Diundecylneopentylamine 395.7 394.7 C27H57N 356,465 0.00163699
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Discussion

Since ancient times, plants or their parts have been used in the treatment of various diseases. The ginger (Zingiber officinale) plant, in addition to its role of flavoring food, has been commonly used for therapeutic purposes (Ghafoor et al. 2020). The therapeutic effect of ginger may be attributed to the bioactive compounds present in it. Our results showed that ZE contained many compounds having medicinal value, such as 1-(4-hydroxy-3-methoxyphenyl)tetradec-4-en3-one Butan-2-one, 4-(3-hydroxy-2-methoxyphenyl)-, which possesses antioxidant and antimicrobial activity (Hwang et al. 2013; Ghasemzadeh et al. 2018), Butan-2-one, 4-(3-hydroxy-2-methoxyphenyl)- which has antimicrobial activity (Ashraf et al. 2017), 1-(4-hydroxy-3-methoxyphenyl)dec-4-en-3-one, which induces apoptosis in human colorectal carcinoma cells via ROS production (Pan et al. 2008), and (3R,5S)-1-(4-hydroxy-3-methoxyphenyl)decane-3,5-diyl diacetate, which is reported to have extracellular melanogenesis inhibition activity (Yamauchi et al. 2019).

Ginger rhizomes are of medicinal importance as they contain bioactive compounds that have a wide range of applications in the pharmaceutical industry (Tomaino et al. 2005). Considering that toltrazuril, the currently used anticoccidial drug for eimeriosis (Alnassan et al. 2013), has side effects in animal tissues and/or in their products, such as eggs, (Dkhil et al. 2015); we prepared AgNPs from ginger rhizomes as a green eco-friendly alternative.

AgNPs showed an anticoccidial effect in the E. papillata-infected mice, which was confirmed in terms of an observed reduction of oocyst count in the feces of treated mice in comparison with that in control mice.

Abdel-Latif et al. (2016) have reported that chitosan activity leads to reduction in the number of oocysts in the feces of E. papillata-infected mice. These observations are also in agreement with results reported by Dkhil et al. (2015) showing berberine to have a similar effect in treating Eimeria infections in mice. In the present study, the treatment of E. papillata-infected mice with biosynthesized AgNPs was shown to reduce the duplication and intracellular development of E. papillata in the jejunal epithelial cells of mice. This action of AgNPs can be considered to contribute to their anti-inflammatory and antioxidant effects.

In the present study, histopathological examination of the jejuna of E. papillata-infected mice showed many lesions, vacuolations of the epithelium, and destruction of certain villi. After treatment with biosynthesized AgNPs, histological changes were significantly improved in the jejuna of the infected mice. Thagfan et al. (2021) found similar ameliorative effects of Morus nigra leaf extracts on the histology of the jejunal epithelium of E. papillata-infected mice. Thagfan et al. (2021) and Alkhudhayri et al. (2018) reported a similar improvement of histopathological changes in the jejunum of E. papillata-infected mice on treatment with selenium nanoparticles.

Goblet cells found in the intestine secrete mucus that acts as an immune-defensive barrier against microbes and parasites that may invade the intestine during food ingestion (Parmar et al. 2021). Many studies have reported that goblet cells are highly affected by Eimeria infection (Dkhil et al. 2013; Kim et al. 1996) In the current study, histological sections of jejuna of E. papillata-infected mice observed on day 5 postinfection showed a reduction in the number of goblet cells (Figs. 7 and 8). Treatment with biosynthesized AgNPs increased the number of goblet cells in the jejuna. In agreement with the results of the present study, the studies by Abdel-Latif et al. (2016) and Alkhudhayri et al. (2018) mentioned previously also report an increase in the number of goblet cells by the action of chitosan and selenium nanoparticles, respectively, in E. papillata-infected mice. Cheng and Leblond (1974) suggested that parasite infection may impair the stem cells found in intestinal crypts that produce goblet cells and this phenomenon could be considered as the reason for the reduction in the number of goblet cells. Interestingly, Alkhudhayri et al. (2018) reported upregulation of the goblet cell-specific gene Muc2 in mice treated with selenium nanoparticles.

Conclusion

This study showed biosynthesized AgNPs to be effective against E. papillata infection in mice. The action of biosynthesized AgNPs was shown to reduce the invasion of E. papillata in the jejunal epithelia and result in enhanced killing of E. papillata at different stages, which was confirmed in terms of low oocyst output in feces of infected mice. More studies are required to cover all aspects of biosynthesized AgNP treatment of infected mice, including analysis of ultrastructural changes in the jejunal epithelia, oxidative stress, and other effects at the molecular level. Moreover, future research should also focus on molecular analysis to identify the genes that are controlled during infection.

Supplementary Information

Below is the link to the electronic supplementary material.

11356_2023_25383_MOESM1_ESM.jpg (141.9KB, jpg)

Fig. S1 GC–MS chromatogram for phytochemical compounds in Zingiber officinale extracts. (JPG 142 KB)

11356_2023_25383_MOESM2_ESM.jpg (2.3MB, jpg)

Fig. S2 Histological changes during infection and after treatment with AgNPs. (A) Non-infected jejunum. (B) AgNPs treated jejunum. (C, D) Infected jejunum. Arrow head for parasitic stages of E. papillata (E) Infected-treated Jejunum treated with AgNPs. (F) Infected-treated Jejunum treated with Amp. Sections stained with H&E Scale bar = 50 μm (JPG 2354 KB)

Author contribution

Infection and treatment of animals were performed by M.A.D., E.M.A, F.A.T, A.A.B., and S.E. Biochemical, parasitological, and histological methodology and investigation were carried out by M.A.D., F.A.T., R.A., M.M., M.Y.M., and T.H. Data analysis, software, data curation, and visualization were performed by S.A., F.A.T., R.A., and E.M.A. Writing—reviewing and editing manuscript was performed by M.A.D., R.A., F.A.T., S.A., and M.Y.M. All authors participated in the design and interpretation of the study and approved the final manuscript.

Funding

This study was supported by the Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2023R96), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia, and also was supported by Researchers Supporting Project (RSP2023R25), King Saud University, Riyadh, Saudi Arabia.

Data availability

All relevant data are within the paper.

Declarations

Ethical approval

The experiments were approved (approval no. HU2021/Z/AD/1213–2) by the Committee of Research Ethics for Laboratory Animal Care of the Department of Zoology, Faculty of Science, Helwan University.

Consent to participate

This is not applicable.

Consent for publication

The authors consented.

Conflict of interest

The authors declare no competing interests.

Footnotes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

11356_2023_25383_MOESM1_ESM.jpg (141.9KB, jpg)

Fig. S1 GC–MS chromatogram for phytochemical compounds in Zingiber officinale extracts. (JPG 142 KB)

11356_2023_25383_MOESM2_ESM.jpg (2.3MB, jpg)

Fig. S2 Histological changes during infection and after treatment with AgNPs. (A) Non-infected jejunum. (B) AgNPs treated jejunum. (C, D) Infected jejunum. Arrow head for parasitic stages of E. papillata (E) Infected-treated Jejunum treated with AgNPs. (F) Infected-treated Jejunum treated with Amp. Sections stained with H&E Scale bar = 50 μm (JPG 2354 KB)

Data Availability Statement

All relevant data are within the paper.

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